Migratory flight imposes oxidative stress in bats

Many animal species migrate over long distances, but the physiological challenges of migration are poorly understood. It has recently been suggested that increased molecular oxidative damage might be one important challenge for migratory animals. We tested the hypothesis that autumn migration imposes an oxidative challenge to bats by comparing values of 4 blood-based markers of oxidative status (oxidative damage and both enzymatic and nonenzymatic antioxidants) between Nathusius' bats Pipistrellus nathusii that were caught during migration flights with those measured in conspecifics after resting for 18 or 24 h. Experiments were carried out at Pape Ornithological Station in Pape (Latvia) in 2016 and 2017. Our results show that flying bats have a blood oxidative status different from that of resting bats due to higher oxidative damage and different expression of both non enzymatic and enzymatic antioxidants (glutathione peroxidase). The differences in oxidative status markers varied betwee n sampli ng years and were in depende nt from in dividual body con dition or sex. Our work provides evidence that migratory flight might impose acute oxidative stress to bats and that resting helps animals to recover from oxidative damage accrued en route. Our data suggest that migrating bats and birds might share similar strategies of mitigating and recovering from oxidative stress.     

Sunset-related timing of flight activity in neotropical bats

Summary The times of onset and completion of the hunting flights of three colonies of neotropical bats, each comprising 100–200 individuals, were observed for nine months. The colonies were of different species: Molossus ater (M.a.) and Molossus molossus (M.m.) of the Molossidae, and Myotis nigricans (My. n.) of the Vespertilionidae. Individuals of Phyllostomus hastatus (P.h., Phyllostomidae) were also observed. All the bats roosted in a building near Restrepo, Colombia (4°16N, 73°34W). Times of emergence in the evening and the return of the last animals in the morning were recorded on 2 to 3 successive days each month. For all bats, the emergence time changed in parallel with that of sunset, and the return paralleled sunrise (Fig. 1). Accordingly, the duration of the activity period is positively correlated with the duration of the night. No annual periodic changes in phase (re sunset/sunrise) of the onset and end of flight activity could be demonstrated, but there was a close relationship between the timing of activity and particular light intensities during twilight (Fig. 4). The first flyers of M.a. appear at the highest intensity (30–300 lx) and those of My. n. at the lowest (0.1–5 lx); the last flyers to return appear in the opposite sequence. For each species, the return to the roost usually occurs at a lower intensity than the departure. These findings, made with four neotropical bat species, differ from those of Subbaraj and Chandrashekaran (1977) with the emballonurid bat Taphozous that they studied at 9°58 N in India. The ecological factors that may play a role in timing the flight activity of tropical bats are discussed. Sunset-related timing, based on the combined effect of (a) the circadian oscillation in arousal and (b) the transition during twilight to a light-intensity range with reduced inhibition of activity (lightsampling behavior), tends to be the rule in tropical bats; time-of-day-related timing is the exception.Supported by the Deutsche Forschungsgemeinschaft (Er 59/1-3+6)     

Feeding mechanisms in bats: variation within the constraints of flight

By any standard, bats are a successful group of mammals andthe evolution of flight and echolocation were certainly keyinnovations behind their success. That is only part of the story,however. Bats have diversified into trophic niches that rangefrom insectivory to feeding on blood, fruit, or nectar. Whileflight places fundamental constraints on the shape of the postcranialskeleton, skull shape in bats is remarkably diverse. Morphologicalstudies of individual families and sympatric assemblages demonstratethat variation in skull shape is clearly associated with trophicspecialization. Field experiments demonstrate that species-specificbiting behaviors during feeding are common and analyses indicatethat the evolution of cranial morphology and feeding behaviorare correlated. Modeling experiments further suggest that feeding(loading) behaviors and skull shape are functionally linked.If the skulls of bats are under selective pressure for minimalmass because of the energetic demands of flight, then they maybe more "optimized" to meet mechanical demands than are theskulls of other mammals. This would make bats a unique modelsystem for studying the evolution of diversity in skull shapeand its functional implications for the evolution of feedingstrategies in mammals.     

Aerodynamic corrections for the flight of birds and bats in wind tunnels

Few wind tunnel studies of animal flight have controlled or corrected for distortions to behaviour, physiology or flight aerodynamics representing the difference between flight in the tunnel and flight in free air. Aerodynamic correction factors are derived based on lifting-line theory and the method of images for an animal flying freely within closed- and open-section wind tunnels; the method is very similar to that used to model flight in ground effect, and as in ground effect the corrections to induced drag may be substantial. These correction factors are used to estimate bound wing circulation, drag and mechanical power for comparison with free flight, and to derive testable predictions of optimum flight strategies for an animal in a tunnel. In an open-section tunnel, mechanical power is increased compared to free flight, and the animal should fly at the tunnel centre. In a closed tunnel mechanical power is usually reduced, and substantial savings are available, particularly at low speeds, if the animal flies close to the tunnel roof. Anecdotal observations confirm that birds and bats adopt this strategy. The mechanical power-speed curve in a closed tunnel is flatter than the curve for free flight, and this may explain the flat metabolic power-speed curves for birds and bats obtained in some measurements.     

The evolution of flight in bats: narrowing the field of plausible hypotheses

The evolution of flapping flight in bats from an arboreal gliding ancestor appears on the surface to be a relatively simple transition. However, bat flight is a highly complex functional system from a morphological, physiological, and aerodynamic perspective, and the transition from a gliding precursor may involve functional discontinuities that represent evolutionary hurdles. In this review, I suggest a framework for a comprehensive treatment of the evolution of complex functional systems that emphasizes a mechanistic understanding of the initial state, the final state, and the proposed transitional states. In this case, bats represent the final state and extant mammalian gliders are used as a model for the initial state. To explore possible transitional states, I propose a set of criteria for evaluating hypotheses about the evolution of flight in vertebrates and suggest methods by which we can advance our understanding of the transition from gliding to flapping flight. Although it is impossible ever to know with certainty the sequence of events landing to flapping flight, the field of possibilities can be narrowed to those that maintain the functional continuity of the wing and result in improved aerodynamic performance across this transition. The fundamental differences between gliding and flapping flight should not necessarily be seen as evidence that this transition could not occur; rather, these differences point out compelling aspects of the aerodynamics of animal wings that require further investigation.     

The flight of pipistrelle bats Pipistrellus pipistrellus during pregnancy and lactation

A group of 20 pipistrelle bats were taken into captivity and allowed free flight and association within a flight room where they gave birth to and successfully reared 17 young. The flight of the females was recorded during pregnancy, early lactation and post-lactation by using stroboscopic stereophotogrammetry (153 flights reconstructed in total). During the investigation body mass was altering owing to reproductive condition, and changes in mass were recorded daily for all (adult and juvenile) bats during the entire study period, which lasted from two weeks before the last birth until release, when the oldest baby was 43 days old. All bats were individually marked, and detailed morphological measurements were made. Pregnant and post-lactating bats were heavier than lactating bats, which showed the lowest wingbeat frequencies. The flight speeds of pregnant, lactating and post-lactating bats showed no significant differences, and this may be because the pregnant bats appeared to have a wider scope for selecting flight speed than the other two reproductive groups, or than animals studied previously. The group of bats as a whole decreased flight speed (scaling as M^-043) and increased wingbeat frequency (scaling as M^0.58) as their mass increased. Wingbeat amplitude showed no relation to body mass, wing area or span, flight speed or frequency. A flight performance model applied to the experimental results and optimum flight conditions is used to predict cost of transport and mechanical power for steady flight, and equilibrium wingbeat amplitude which is compared with observations.     

Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii.

The energetic cost of flight in a wind-tunnel was measured at various combinations of speed and flight angle from two species of bats whose body masses differ by almost an order of magnitude. The highest mean metabolic rate per unit body mass measured from P. hastatus (mean body mass, 0.093 kg) was 130.4 Wkg-1, and that for P. gouldii (mean body mass, 0.78 kg) was 69.6 Wkg-1. These highest metabolic rates, recorded from flying bats, are essentially the same as those predicted for flying birds of the same body masses, but are from 2.5 to 3.0 times greater than the highest metabolic rates of which similar-size exercising terrestrial mammals appear capable. The lowest mean rate of energy utilization per unit body mass P. hastatus required to sustain level flight was 94.2 Wkg-1 and that for P. gouldii was 53.4 Wkg-1. These data from flying bats together with comparable data for flying birds all fall along a straight line when plotted on double logarithmic coordinates as a function of body mass. Such data show that even the lowest metabolic requirements of bats and birds during level flight are about twice the highest metabolic capabilities of similar-size terrestrial mammals. Flying bats share with flying birds the ability to move substantially greater distance per unit energy consumed than walking or running mammals. Calculations show that P. hastatus requires only one-sixth the energy to cover a given distance as does the same-size terrestrial mammal, while P. gouldii requires one-fourth the energy of the same-size terrestrial mammal. An empirically derived equation is presented which enables one to make estimates of the metabolic rates of bats and birds during level flight in nature from body mass data alone. Metabolic data obtained in this study are compared with predictions calculated from an avian flight theory.     

Ethanol ingestion affects flight performance and echolocation in Egyptian fruit bats

Ethanol, a potential toxin for vertebrates, is present in all fleshy fruits and its content increases as the fruit ripens. Previously, we found that the marginal value of food for Egyptian fruit bats, Rousettus aegyptiacus, decreases when its ethanol content exceeds 1%. Therefore, we hypothesized that, if ingested, food containing >1% ethanol is toxic to these bats, probably causing inebriation that will affect flight and echolocation skills. We tested this hypothesis by flying Egyptian fruit bats in an indoor corridor and found that after ingesting ethanol-rich food bats flew significantly slower than when fed ethanol-free food. Also, the ingestion of ethanol significantly affected several variables of the bats’ echolocation calls and behavior. We concluded that ethanol can be toxic to fruit bats; not only does it reduce the marginal value of food, but it also has negative physiological effects on their ability to fly competently and on their calling ability.     

Commuting fruit bats beneficially modulate their flight in relation to wind

When animals move, their tracks may be strongly influenced by the motion of air or water, and this may affect the speed, energetics and prospects of the journey. Flying organisms, such as bats, may thus benefit from modifying their flight in response to the wind vector. Yet, practical difficulties have so far limited the understanding of this response for free-ranging bats. We tracked nine straw-coloured fruit bats (Eidolon helvum) that flew 42.5 ± 17.5 km (mean ± s.d.) to and from their roost near Accra, Ghana. Following detailed atmospheric simulations, we found that bats compensated for wind drift, as predicted under constant winds, and decreased their airspeed in response to tailwind assistance such that their groundspeed remained nearly constant. In addition, bats increased their airspeed with increasing crosswind speed. Overall, bats modulated their airspeed in relation to wind speed at different wind directions in a manner predicted by a two-dimensional optimal movement model. We conclude that sophisticated behavioural mechanisms to minimize the cost of transport under various wind conditions have evolved in bats. The bats’ response to the wind is similar to that reported for migratory birds and insects, suggesting convergent evolution of flight behaviours in volant organisms.     

The evolution of flight and echolocation in bats: another leap in the dark

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.     

Uniform myosin isoforms in the flight muscles for little brown bats, Myotis lucifugus

The present study used muscle histochemistry and polyacrylamide gel electrophoresis of native myosin and myosin heavy chains to establish a correlation, if any, between chiropteran histochemical fiber types and myosin isoform composition. Histochemical analysis of the primary flight muscle, the pectoralis profundus, documented the presence of a single histochemical fiber type, here termed Type II. Electrophoresis of native myosin isolated from pectoralis muscle yielded a single isoform that comigrated with the FM-3 isoform of rat diaphragm. Heavy chain analysis of the Myotis pectoralis demonstrated a single heavy chain with comparable electrophoretic mobility to rat IIa myosin heavy chain. These data demonstrate unique histochemical and biochemical homogeneity in the myosin composition of the pectoralis muscle of Myotis lucifugus. Thus this muscle is extremely specialized for flight at histochemical, morphologic, and molecular levels. These data contrast with the mixed myosin and histochemical fiber types found in other mammals, as well as in other muscles of Myotis lucifugus.     

Paleoecology of early middle Eocene bats from Messel,FRG. aspects of flight,feeding and echolocation

By their diversified flight apparatus Messel bats occupied specific flight niches similar to those of extant tropical bats. The small Palaeochiropteryx tupaiodon is considered to be most specialized for hunting close to the ground and for hovering inside dense vegetation. Contrarily, Hassianycteris spp. most likely were high and fast flyers in the open space.

The analysis of gut contents proves that Palaeochiropteryx spp. exclusively fed on small moths and caddis flies, i.e. slow and low flying insects. For P. tupaiodon this confirms the foraging strategy independently from wing morphology. Hassianycteris spp. preyed mainly on beetles or other insects with thick cuticules.

Inner ears of Messel microbats are less specialized compared to those of recent species. Especially P. tupaiodon shows no acoustical specialization with regard to its hunting habitat. Thus, we assume that during the early evolution of bats the development of different flight styles and wing shapes preceded acoustical refinements of the echolocation system.